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Diversity and Evolution of Bodyguard Manipulation. Fanny Maure, Simon Payette Daoust, Jacques Brodeur, Guillaume Mitta, Frédéric Thomas

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Diversity and Evolution of Bodyguard Manipulation. Fanny Maure, Simon Payette Daoust, Jacques Brodeur, Guillaume Mitta, Frédéric Thomas Diversity and evolution of bodyguard manipulation. Fanny Maure, Simon Payette Daoust, Jacques Brodeur, Guillaume Mitta, Frédéric Thomas To cite this version: Fanny Maure, Simon Payette Daoust, Jacques Brodeur, Guillaume Mitta, Frédéric Thomas. Diversity and evolution of bodyguard manipulation.. Journal of Experimental Biology, Cambridge University Press, 2013, 216 (Pt 1), pp.36-42. 10.1242/jeb.073130. halsde-00771849 HAL Id: halsde-00771849 https://hal.archives-ouvertes.fr/halsde-00771849 Submitted on 7 Aug 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. 36 The Journal of Experimental Biology 216, 36-42 © 2013. Published by The Company of Biologists Ltd doi:10.1242/jeb.073130 REVIEW Diversity and evolution of bodyguard manipulation Fanny Maure1,2,*,†, Simon Payette Daoust1,2,*, Jacques Brodeur2, Guillaume Mitta3 and Frédéric Thomas1 1IRD, MIVEGEC (UMR CNRS/IRD/UM1/UM2), 911 Avenue Agropolis, BP 64501, FR-34394 Montpellier cedex 5, France, 2Institut de recherche en biologie végétale, Département de sciences biologiques, Université de Montréal 4101, rue Sherbrooke est, Montréal, Québec, Canada H1X 2B2 and 3Université de Perpignan Via Domitia, Écologie et Évolution des Interactions (UMR CNRS 5244), 52 Avenue Paul Alduy, 66860 Perpignan cedex, France *These authors contributed equally to this work †Author for correspondence ([email protected]) Summary Among the different strategies used by parasites to usurp the behaviour of their host, one of the most fascinating is bodyguard manipulation. While all classic examples of bodyguard manipulation involve insect parasitoids, induced protective behaviours have also evolved in other parasite–host systems, typically as specific dimensions of the total manipulation. For instance, parasites may manipulate the host to reduce host mortality during their development or to avoid predation by non-host predators. This type of host manipulation behaviour is rarely described, probably due to the fact that studies have mainly focused on predation enhancement rather than studying all the dimensions of the manipulation. Here, in addition to the classic cases of bodyguard manipulation, we also review these ʻbodyguard dimensionsʼ and propose extending the current definition of bodyguard manipulation to include the latter. We also discuss different evolutionary scenarios under which such manipulations could have evolved. Keywords: host–parasite relationships, co-evolution, bodyguard manipulation, bodyguard dimension. Received 28 March 2012; Accepted 30 May 2012 Introduction to vertebrate hosts by blood-sucking insects such as mosquitoes Host manipulation by parasites is one of the most concrete and (Lefèvre et al., 2006). In this situation, transmission opportunities fascinating examples of the extended phenotype (Dawkins, 1982). for the parasite increase with the number of potential hosts visited Parasites across many taxa, from viruses to parasitoids, have by the mosquitoes, and parasites have been shown to shorten the evolved the ability to manipulate their hosts to their own advantage, duration of individual blood meals to increase the number of hosts sometimes inducing spectacular behavioural changes in their hosts attacked (Moore, 1993; Koella et al., 1998). (Moore, 2002; Lefèvre et al., 2009; Poulin, 2010; Hughes et al., The last category of manipulation is known as bodyguard 2012). Although these phenotypic changes occur only in parasitized manipulation. Although fascinating, it remains largely unstudied, hosts, evidence of benefits for the parasites is necessary to allow with only a handful of documented cases and even fewer addressing conclusions to be drawn about their adaptiveness (Poulin, 2010). the underlying mechanisms. This type of manipulation is used by Traditionally, parasitic host manipulations have been divided insect parasitoids that must exit their host following larval into four general categories, three of which have been well development and pupate on external substrates, and is defined by documented (Poulin, 2010). In the first, the parasites can Poulin as ‘a manipulation that alters the behaviour of the host in manipulate their hosts in such a way as to favour transmission to ways that will provide protection to the parasite pupae from their next host, by rendering the former more susceptible to predators or other dangers’ (Poulin, 2010), where the host forgoes predation. One of the best-described examples is that of amphipods potential foraging and/or reproductive opportunities. While all of infected with trematode parasites; infected gammarids display an the documented examples of bodyguard manipulation involve aberrant escape response toward the water surface following a parasitoids and more particularly parasitic wasps, induced mechanical disturbance, and remain at the air–water interface, protective behaviours can evolve in other parasite–host systems. thereby favouring the parasite’s transmission to the definitive host, For instance, within the context of multidimensional manipulations, a waterfowl (Bethel and Holmes, 1977; Helluy, 1983; Helluy, where parasites modify multiple aspects of their host’s phenotype 1984). The second category involves parasites that must either exit (see Appendix), certain dimensions (i.e. aspects) of these the host or release their propagules in a habitat other than the one manipulations have been shown to reduce predation pressure and in which the host lives. For example, crickets Nemobius sylvestris therefore the mortality of the immature parasites. Although infected with the nematomorph Paragordius tricuspidatus were currently labelled as the ‘predation suppression’ phase (see Parker shown to actively jump into pools and streams, where the worms et al., 2009), these behaviours ultimately ensure parasite survival. would egress from the host and find mates (Thomas et al., 2002b). From this point of view, they could be interpreted as ‘bodyguard The third type of manipulation involves vector-borne parasite dimensions’, where manipulated hosts act as bodyguards only transmission. The best-known examples are pathogens transmitted during specific phases of the manipulation. THE JOURNAL OF EXPERIMENTAL BIOLOGY Bodyguard manipulation 37 The present review examines the diversity and evolution of beetle Coleomegilla maculata (Table1). Female wasps lay a single bodyguard manipulation. First, we will give an overview of the egg in the host and the parasitoid larva grows inside the body cavity textbook cases of bodyguard manipulation. Second, we will of the ladybird until it reaches the prepupal stage. Then, the larva highlight the bodyguard dimension that occurs in a great number egresses from its host and begins spinning a cocoon between the of biological systems, and discuss its potential inclusion in a ladybird’s legs (Fig.1C). Remarkably for a parasitoid, D. broader definition of bodyguard manipulation. We will conclude coccinellae does not kill its host at the end of its development; this paper by discussing the evolutionary process leading to instead, it partially paralyses the coccinellid upon egression. Thus bodyguard manipulation. positioned on top of the parasitic wasp cocoon and displaying little twitching when disturbed, the ladybird acts as a bodyguard for the Textbook cases of bodyguard manipulation pupating wasp against predators (Maure et al., 2011). Moreover, it In contrast to most true parasites, insect parasitoids are of relatively is likely that the aposematic coloration of the ladybirds (Marples et large size and possess a free-living adult stage, and their al., 1994) operates as a complementary protection for the parasitoid, development almost universally kills the host (but see English-Loeb depending on the nature of the predators. Thus, D. coccinellae et al., 1990; Maure et al., 2011). Because of these characteristics, could also potentially usurp the natural defences of its host. behavioural modifications induced by parasitoids have evolved in a way that increases their survival during pupation (i.e. when the Indirect protection parasitoid is at its most vulnerable), through an efficient protection In contrast to the previous examples where manipulated hosts against natural enemies or abiotic factors (Poulin et al., 1994; played an active and direct role against natural enemies of the Brodeur and Boivin, 2004). The induced protection conferred by parasitoid, the following studies describe cases where the host is the host can be either direct or indirect, depending on whether the manipulated prior to parasitoid pupation in order to provide shelter onset of manipulation coincides with the period of high against potential biotic and abiotic threats. Although these vulnerability (direct protection) or occurs just before this period bodyguards do not directly face the threats, the benefits for (indirect protection). In the first case, the host is maintained alive, parasitoid survival are equally important. at least until the beginning of parasitoid pupal development, in With their studies on the aphid parasitoid Aphidius nigripes,
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